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Journal of Integrative Agriculture  2018, Vol. 17 Issue (09): 1991-1998    DOI: 10.1016/S2095-3119(17)61878-1
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Dynamics of Bt cotton Cry1Ac protein content under an alternating high temperature regime and effects on nitrogen metabolism
ZHANG Xiang1, 2, RUI Qiu-zhi1, LIANG Pan-pan1, WEI Chen-hua1, DENG Guo-qiang1, CHEN Yuan1, CHEN Yuan1, DONG Zhao-di1, CHEN De-hua1#br#
1 Key Laboratory of Crop Genetics and Physiology of Jiangsu Province, Yangzhou University, Yangzhou 225009, P.R.China
2 Plant Genome Mapping Laboratory, University of Georgia, Athens 30605, USA
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Abstract  This study was conducted to investigate the effects of alternating high temperature on Cry1Ac protein content on Bt cotton cultivars Sikang 1 (SK-1, a conventional cultivar) and Sikang 3 (SK-3, a hybrid cultivar). In 2011 and 2012, cotton plants were subjected to high temperature treatments ranging from 32 to 40°C in climate chambers to investigate the effects of high temperature on boll shell insecticidal protein expression. The experiments showed that significant decline of the boll shell insecticidal protein was detected at temperatures higher than 38°C after 24 h. Based on the results, the cotton plants were treated with the threshold temperature of 38°C from 6:00 a.m. to 6:00 p.m. followed by a normal temperature of 27°C during the remaining night hours (DH/NN) in 2012 and 2013. These treatments were conducted at peak boll growth stage for both cultivars in study periods of 0, 4, 7, and 10 d. Temperature treatment of 32°C from 6:00 a.m. to 6:00 p.m. and 27°C in the remaining hours was set as control. The results showed that, compared with the control, after the DH/NN stress treatment applied for 7 d, the boll shell Cry1Ac protein content level was significantly decreased by 19.1 and 17.5% for SK-1 and by 15.3 and 13.7% for SK-3 in 2012 and 2013, respectively. Further analysis of nitrogen metabolic physiology under DH/NN showed that the soluble protein content and the glutamic pyruvic transaminase (GPT) activities decreased slightly after 4 d, and then decreased sharply after 7 d. The free amino acid content and the protease content increased sharply after 7 d. The changes in SK-1 were greater than those in SK-3. These results suggest that under DH/NN stress, boll shell Cry1Ac protein content decline was delayed. Reduced protein synthesis and increased protein degradation in the boll shell decreased protein content, including Bt protein, which may reduce resistance to the cotton bollworm.
Keywords:  Bt cotton        alternating temperature        Cry1Ac protein        nitrogen metabolism  
Received: 29 September 2017   Accepted:
Fund: This work was supported by the National Natural Science Foundation of China (31471435, 31671613, and 31301263), the China Postdoctoral Science Foundation Grant (2016M591934), the Postdoctoral Science Foundation Grant in Jiangsu Province, China (1601116C), the Key Projects of Natural Science Research in Colleges and Universities of Jiangsu, China (17KJA210003), a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions, China (PAPD), and the Practice Innovation Training Project for College Students in Jiangsu Province, China.
Corresponding Authors:  Correspondence CHEN De-hua,Tel:+86-514-87979357,Fax:+86-514-87996817,   
About author:  ZHANG Xiang,Tel:+86-514-87979357,;

Cite this article: 

ZHANG Xiang, RUI Qiu-zhi, LIANG Pan-pan, WEI Chen-hua, DENG Guo-qiang, CHEN Yuan, CHEN Yuan, DONG Zhao-di, CHEN De-hua. 2018. Dynamics of Bt cotton Cry1Ac protein content under an alternating high temperature regime and effects on nitrogen metabolism. Journal of Integrative Agriculture, 17(09): 1991-1998.

Adamczyk J J, Hardee D D, Adams L C V, Sumerford D. 2001. Correlating differences in larval survival and development of bollworm (Lepidoptera: Noctuidae) and fall armyworm (Lepidoptera: Noctuidae) to differential expression of Cry1A(c) delta-endotoxin in various plant parts among commercial cultivars of transgenic Bacillus thuringiensis cotton. Journal of Economic Entomology, 94, 284–290.
Bakhsh A, Shahzad K, Husnain T. 2011. Variation in the spatio-temporal expression of insecticidal genes in cotton. Czech Journal of Genetics and Plant Breeding, 47, 1–9.
Blaise D, Kranthi K R. 2011. Cry1Ac expression in transgenic Bt cotton hybrids is influenced by soil moisture and depth. Current Science, 101, 783–786.
Bradford M M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.
Chen D H, Ye G Y, Yang C Q, Chen Y, Wu Y K. 2005a. Effect of introducing Bacillus thuringiensis gene on nitrogen metabolism in cotton. Field Crops Research, 92, 1–9.
Chen D H, Ye G Y, Yang C Q, Chen Y, Wu Y K. 2005b. The effect of high temperature on the insecticidal properties of Bt cotton. Environmental and Experimental Botany, 53, 333–342.
Chen S, Wu J Y, Cheng D R, Zhang R X, Huang J Q. 1999. On the enzyme-linked immunosorbent assay of Bacillus thuringiensis insecticidal protein expressed in transgenic cotton. Acta Gossypii Sinica, 11, 259–267. (in Chinese) 
Chen Y, Han Y, Wang J, Hua M M, Gu C, Li G S, Zhang X, Chen D H. 2014. Effects of high temperature on Bt proteins expression and nitrogen metabolic physiology in square of Bt cotton at the peak squaring stage. Chinese Journal of Applied Ecology, 25, 2623–2628. (in Chinese)
Chen Y, Wen Y, Chen Y, Zhang X, Wang Y, Chen D. 2013. The recovery of Bt toxin content after temperature stress termination in transgenic cotton. Spanish Journal of Agricultural Research, 11, 438.
Chen Y, Wen Y J, Chen Y, Cothren J T, Zhang X, Wang Y H, Payne W A, Chen D H. 2012. Effects of extreme air temperature and humidity on the insecticidal expression level of Bt cotton. Journal of Integrative Agriculture, 11, 1836–1844.
Chen Y, Wen Y J, Zhang X, Chen D H. 2012. The effects of the relative humidity on the insecticidal expression level of Bt cotton during bolling period under high temperature. Field Crops Research, 137, 141–147.
Dadgale P R, Chavan D A, Gudade B A, Jadhav S G, Deshmukh V A, Pal S. 2014. Productivity and quality of Bt cotton (Gossypium hirsutum) as influenced by planting geometry and nitrogen levels under irrigated and rainfed conditions. Indian Journal of Agricultural Sciences, 84, 1069–1072.
Dong H Z, Li W J, Tang W, Li Z H, Zhang D M. 2007. Heterosis in yield, endotoxin expression and some physiological parameters in Bt transgenic cotton. Plant Breeding, 2007, 169–175.
Gujar G T, Kalia V, Bunker G K, Dhurua S. 2010. Impact of different levels of non-Bt cotton refuges on pest populations, bollworm damage, and Bt cotton production. Journal of Asia-Pacific Entomology, 13, 249–253.
Hallikeri S S, Halemani H L, Patil B C, Nandagavi R A. 2011. Influence of nitrogen management on expression of cry protein in Bt-cotton (Gossypium hirsutum). Indian Journal of Agronomy, 56, 62–67.
Ian J R. 2006. Effect of genotype, edaphic, environmental conditions, and agronomic practices on CryIAc protein expression in transgenic cotton. The Journal of Cotton Science, 10, 252–262.
Jessen D L, Bames D K, Vance C P. 1988. Bidirectional selection in alfalfa for activity of nodule nitrogen and carbon-assimilating enzymes. Crop Science, 28, 18–22.
Jiang L J, Duan L S, Tian X L, Wang B M, Zhang H F, Zhang M C, Li Z H. 2006. NaCl salinity stress decreased Bacillus thuringiensis (Bt) protein content of transgenic Bt cotton (Gossypium hirsutum L.) seedlings. Environmental and Experimental Botany, 55, 315–320.
Jiang Z G, Zhang Y Z, Feng M S, Chen Y, Zhang X, Chen D H. 2012. Effect of high temperature on the insecticidal properties and nitrogen metabolismin Bt cotton at peak bolling stage. China Cotton, 39, 13–32. (in Chinese)
Luo Z, Dong H H, Li W J, Ming Z, Zhu Y Q. 2008. Individual and combined effects of salinity and waterlogging on Cry1Ac expression and insecticidal efficacy of Bt cotton. Crop Protection, 27, 1485–1490.
Lü C H. 2013. The effect of high temperature on the insecticidal proterties and nitrogen metabolism of Bt cotton reproductive organ. MSc thesis, Department of Agronomy, Yangzhou University. (in Chinese)
Martins C M, Beyene G, Hofs J L, Krueger K, Van D V C, Schlueter U, Kunert K J. 2008. Effect of water-deficit stress on cotton plants expressing the Bacillus thuringiensis toxin. Annals of Applied Biology, 152, 255–262.
Rui C H, Fan X L, Dong F S, Guo S D. 2002. Temporal and spatial dynamics of the resistance of transgenic cotton cultivars to Helicoverpa armigera (Hübner). Acta Entomologica Sinica, 37, 1699–1705. (in Chinese)
Russell D, Deguine J P. 2006. Sustainability of Bt cotton in China and India. Cahiers Agricultures, 15, 54–59.
Saini M K, Dhawan A K. 2014. Effect of nitrogen fertigation and sowing time on the expression of Cry2Ab and on mortality of Spodoptera litura in Bollgard II cotton. Journal of Environmental Biology, 35, 311–315.
Steward F C. 1965. Metabolism of nitrogenous compounds. In: Treatise A, Steward F C, eds., Plant Physiology. Academic Press, New York. pp. 1128–1136.
Thomas H. 1975. Regulation of alanine aminotransferase in leaves of Lolium temulentum during senescence. Zeitschrift für Pflanzenphysiologie, 74, 208–218.
Vance C P, Heichel G H, Barnes D K, Bryan J M, Johnson L E. 1979. Nitrogen fixation, nodule development, and vegetative regrowth of alfalfa (Medicago sativa L.) following harvest. Plant Physiology, 64, 1–8.
Wang H L, Gan Y T, Wang R Y, Niu J Y, Zhao H, Yang Q G, Li G C. 2008. Phenological trends in winter wheat and spring cotton in response to climate changes in northwest China. Agricultural and Forest Meteorology, 148, 1242–1251.
Wei H, Zhao W Q, Yang J H, Derrick M O, Dimintra A L, Zhou Z G. 2016. Relationship between potassium fertilization and nitrogen metabolism in the leaf subtending the cotton (Gossypium hirsutum L.) boll during the boll development stage. Plant Physiology and Biochemistry, 101, 113–123.
Weiler E W, Jourdan P S, Conrad W. 1981. Levels of indole-3-acetic acid in intact and decapitated coleoptiles as determined by a specific and highly sensitive solid-phase enzyme immunoassay. Planta, 153, 561–571.
Zhang B H. 2013. Transgenic cotton: from biotransformation methods to agricultural application. Methods in Molecular Biology, 958, 3–15.
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